Whole genome comparisons of montane hummingbirds reveal targets of natural selection during independent high-altitude colonizations

Organisms inhabiting high-altitude environments experience physiological stressors including reduced oxygen availability, cold, and UV exposure. Despite these extreme conditions, hummingbirds are diverse and abundant in the... [ view full abstract ]

Organisms inhabiting high-altitude environments experience physiological stressors including reduced oxygen availability, cold, and UV exposure. Despite these extreme conditions, hummingbirds are diverse and abundant in the high Andes. The intense aerobic requirements necessary for hovering flight exacerbate the high-altitude physiological challenge, creating conditions favorable for genetic adaptation. To examine the mechanisms underlying this adaptation we used whole genome sequencing to compare two high altitude species of hummingbird (Oreotrochilus melanogaster, max. elevation 5,000 m; and Colibri coruscans, max. elevation 4,000 m) to five lowland species of hummingbirds (Florisuga mellivora, Glaucis hirsutus, Calypte anna, Thalurania furcata, and Schistes geoffroyi) and two swift species as an outgroup (Chaetura vauxi, Chaetura pelagica). The black-breasted hillstar (O. melanogaster) was sequenced to ~130X coverage and de novo assembled. The remaining species were sequenced to ~15-35X or had publically available reference genomes. Signatures of positive selection were detected using a branch-site model or were inferred from gene family expansions. Candidate genes identified in O. melanogaster are involved in a variety of hypoxia-related physiological and cellular pathways, including: oxygen binding, angiogenesis, cardiac and pulmonary function, cellular respiration, vasodilation, cold metabolism, and UV damage repair. The catabolic process GO term, which is known to be involved in the cellular response to hypoxia in other organisms, was statistically enriched in O. melanogaster. Conversely, candidate genes for C. coruscans are involved in hemostasis. No shared candidate genes or molecular pathways were identified between the two high-altitude hummingbird species. The large number of candidate genes identified in known hypoxia-related pathways in O. melanogaster, but not C. coruscans, may result from the extreme high-altitude habitat of the black-breasted hillstar and may represent a physiological limit that necessitated adaptive change.